Research Advances in Potassium Ion Channel AKT1 in Plant

doi:10.13560/j.cnki.biotech.bull.1985.2019-0033

Abstract

Abstract:

As one of 3 essential nutrients for plant growth and development,potassium（K）plays an crucial role in regulating enzyme activity,membrane potential,cell homeostasis,and protein stable synthesis. K⁺uptake and transport in plant is via potassium channels and transporters. In recent years,different types of potassium channels have been isolated. The earliest discovered and most studied potassium channel is the Shaker potassium channel. This paper introduces the potassium channel in plant in aspects of its classification,the structural characteristics of the Shaker potassium channel,the effects of AKT1 on plant growth and development,the function of AKT1 under abiotic stress and biotic stress,and 2 internal regulation mechanisms of potassium channel AKT1 by CBL/CIPK phosphorylation and heteromerization. The paper also prospects the future issues in studying the potassium channel AKT1.

Key words: potassium ion, potassium ion channel, AKT1, regulation

YANG Ling-qin, LIU Jing, LI Wei, DAI Liang-ying. Research Advances in Potassium Ion Channel AKT1 in Plant[J]. Biotechnology Bulletin, 2019, 35(4): 94-100.

References

[1] Ingo D, Nobuyuki U.Potassium channels in plant cells[J]. Febs Journal, 2011, 278(22):4293-4303.
[2] Amtmann A, Troufflard S, Armengaud P .The effect of potassium nutrition on pest and disease resistance in plants[J]. Physiologia Plantarum, 2008, 133(4):682-691.
[3] Wyn Jones RG, Pollard A.Proteins, enzymes and inorganic ions[M]// Lauchli A, Pirson A. Encyclopedia of Plant Physiology. Berlin:Springer, 1983:528-526.
[4] Schroeder J I, Ward J M, Gassmann W.Perspectives on the physiology and structure of inward-rectifying K+ channels in higher plants:biophysical implications for K+ uptake[J]. Annu Rev Biophys Biomol Struct, 1994, 23(1):441-471.
[5] Schroeder JI, Hedrich R, Fernandez J M.Potassium-selective single channels in guard cell protoplasts of Vicia faba[J]. Nat, 1984, 312(5992):361-362.
[6] Dennison KL, Robertson WR, et al.Functions of AKT1 and AKT2 potassium channels determined by studies of single and double mutants of Arabidopsis[J]. Plant Physiol, 2001, 127(3):1012-1019.
[7] 闵水珠. 植物钾离子通道的分子生物学研究进展[J]. 浙江农业学报, 2005, 17(3):163-169.
[8] 吴平, 印莉萍, 张立平, 等. 植物营养分子生理学[M]. 北京:科学出版社, 2001, 163-211
[9] 程钰宏, 赵瑞雪, 董宽虎. 植物钾(K+)离子通道的研究[J]. 山西农业科学, 2008, 36(2):3-7.
[10] Fan LM, Zhao Z, Assmann S, et al.Guard cells:a dynamic signa-ling model[J]. Curr Opin Plant Biol, 2004, 7(5):537-546.
[11] Tripti Sharma IDJR.The role of K+ channels in uptake and redistr-ibution of potassium in the model plant Arabidopsis thaliana[J]. Front Plant Sci, 2013, 4(2):224-224.
[12] Gambale F, Uozumi N.Properties of shaker-type potassium channels in higher plants[J]. J Membr Biol, 2006, 210(1):1-19.
[13] Czempinski K, Zimmermann S, Ehrhardt T, et al.New structure and function in plant K+ channels:KCO1, an outward rectifier with a steep Ca²+ dependency[J]. EMBO J, 1997, 16(10):2565-2575.
[14] Czempinski K, Zimmermann S, Muller-Rober BN.Molecular mechanisms and regulation of plant ion channels[J]. J Exp Bot, 1999, 50(Special):955-966.
[15] Marcel D, Müller T, Hedrich R, et al.K+ transport characteristics of the plasma membrane tandem-pore channel TPK4 and pore chimeras with its vacuolar homologs[J]. Febs Letters, 2010, 584(11):2433-2439.
[16] Voelker C, Gomez-Porras JL, Becker D, et al.Roles of tandem-pore K+, channels in plants - a puzzle still to be solved[J]. Plant Biology, 2010, 12(s1):56-63.
[17] Sentenac H, Bonneaud N, Minet M, et al.Cloning and expression in yeast of a plant potassium ion transport system[J]. Science, 1992, 256(5057):663-665.
[18] Nieves-Cordones M, Chavanieu A, et al.Distinct amino acids in the C-linker domain of the Arabidopsis K+ channel KAT2 determine its subcellular localization and activity at the plasma membrane[J]. Plant Physiol, 2014, 164(3):1415-1429.
[19] Nieves-Cordones M, Gaillard I.Involvement of the S4-S5 linker and the C-linker domain regions to voltage-gating in plant Shaker channels:Comparison with animal HCN and Kv channels[J]. Plant Signaling & Behavior, 2014, 9(10):e972892.
[20] Xu J, Li HD, Chen LQ, et al.A protein kinase, interacting with two calcineurin B-like proteins, regulates K+ transporter AKT1 in Arabidopsis[J]. Cell, 2006, 125(7):1347-1360.
[21] Benito B, Haro R, Amtmann A, et al.The twins K+ and Na+ in plants[J]. J Plant Physiol, 2014, 171(9):723-731.
[22] Gambale F, Uozumi N.Properties of Shaker-type potassium channels in higher plants[J]. J Membr Biol, 2006, 210(1):1-19
[23] 李娟. 水稻钾离子通道OsAKT1及其调控因子参与水稻钾吸收的实验证据[D]. 北京:中国农业大学, 2014.
[24] Ardie SW, Liu SK, Takano T.Expression of the AKT1-type K+ channel gene from Puccinellia tenuiflora, PutAKT1, enhances salt tolerance in Arabidopsis[J]. Plant Cell Rep, 2010, 29(8):865-874.
[25] Spalding EP, Hirsch RE, Lewis DR, et al.Potassium uptake supporting plant growth in the absence of AKT1 channel activity[J]. J Gen Physiol, 1999, 113(6):909-918.
[26] Hirsch RE, Sussman MR.A role for the AKT1 potassium channel in plant nutrition[J]. Science, 1998, 280(5365):918-921.
[27] Ache P, Becker D, Deeken R, et al.VFK1, a Vicia faba K+ channel involved in phloem unloading[J]. Plant J, 2015, 27(6):571-580.
[28] Adams E, Miyazaki T, Shin R.Contribution of KUPs to potassium and cesium accumulation appears complementary in Arabidopsis[J]. Plant Signaling & Behavior, 2018:1-3.
[29] Adams E, Miyazaki T, et al.Cesium inhibits plant growth primarily through reduction of potassium influx and accumulation in Arabidopsis[J]. Plant Cell Physiol, 2018, 60(1):63-76.
[30] Rodrígueznavarro A, Rubio F.High-affinity potassium and sodium transport systems in plants[J]. J Exp Bot, 2006, 57(5):1149-1160.
[31] Wu GQ, Feng RJ, et al.Sodium chloride stimulates growth and alleviates sorbitol-induced osmotic stress in sugar beet seedlings[J]. Plant Growth Regulation, 2015, 75(1):307-316.
[32] Ahmad I, Mian A, Maathuis FJM.Overexpression of the rice AKT1 potassium channel affects potassium nutrition and rice drought tolerance[J]. J Exp Bot, 2016, 67(9):2689-2698.
[33] Nieves-Cordones M, Caballero F, Martínez V, et al.Disruption of the Arabidopsis thaliana inward-rectifier K+ channel AKT1 improves plant responses to water stress[J]. Plant & Cell Physiology, 2012, 53(2):423-432.
[34] Flowers TJ.Improving crop salt tolerance[J]. J Exp Bot, 2004, 55(396):307-319.
[35] Zhang JL, Shi H.Physiological and molecular mechanisms of plant salt tolerance[J]. Photosynthesis Research, 2013, 115(1):1-22.
[36] Assaha DVM, Akihiro U, Hirofumi S, et al.The role of Na+ and K+ transporters in salt stress adaptation in glycophytes[J]. Frontiers in Physiology, 2017, 8:509-509.
[37] Nievescordones M, Miller AJ, Alemán F, et al.A putative role for the plasma membrane potential in the control of the expression of the gene encoding the tomato high-affinity potassium transporter HAK5[J]. Plant Molecular Biology, 2008, 68(6):521-532
[38] D Golldack, F Quigley, CB Michalowski, et al. Salinity stress-tolerant and -sensitive rice(Oryza sativa L.)regulate AKT1-type potassium channel transcripts differently[J]. Plant Molecular Biology, 2003, 51(1):71-81.
[39] Wang N, Qiao W, Liu X, et al.Relative contribution of Na+/K+ homeostasis, photochemical efficiency and antioxidant defense system to differential salt tolerance in cotton(Gossypium hirsutum L.)cultivars[J]. Plant Physiol Biochem, 2017, 119:121-131.
[40] Duan HR, Ma Q, Zhang JL, et al.The inward-rectifying K+, channel SsAKT1 is a candidate involved in K+, uptake in the halophyte Suaeda salsa, under saline condition[J]. Plant and Soil, 2015, 395(1-2):173-187.
[41] Ardie SW, Liu S, Takano T.Expression of the AKT1-type K(+)channel gene from Puccinellia tenuiflora, PutAKT1, enhances salt tolerance in Arabidopsis[J]. Plant Cell Rep, 2010, 29(8):865-874.
[42] Harrewijn P.Potassium and plant health[J]. European Journal of Plant Pathology, 1979, 85(2):82-82.
[43] Li J, Long Y, Qi G N, et al.The Os-AKT1 channel is critical for K+ uptake in rice roots and is modulated by the rice CBL1-CIPK23 complex[J]. Plant Cell, 2014, 26(8):3387-3402.
[44] Shi X, Long Y, He F, et al.The fungal pathogen Magnaporthe oryzae suppresses innate immunity by modulating a host potassium channel[J]. PLoS Pathogens, 2018, 14(1):e1006878.
[45] 刘晓燕, 何萍, 金继运. 钾在植物抗病性中的作用及机理的研究进展[J]. 植物营养与肥料学报, 2006, 12(3):445-450.
[46] Lozovaya VV, Lygin AV, Li S, et al.Biochemical response of soybean roots to, Fusarium solani, f. sp. glycines, Infection[J]. Crop Science, 2004, 44(3):819-826.
[47] 龙雨. 水稻钾离子通道OsAKT1生理功能及其调控机制的电生理学研究[D]. 北京:中国农业大学, 2014.
[48] Mühlhäuser WW, Hörner M, Weber W, et al.Light-regulated protein kinases based on the CRY2-CIB1 system[J]. Methods in Molecular Biology, 2017, 1596:257-270.
[49] Nagae M, Nozawa A, Koizumi N, et al.The crystal structure of the novel calcium-binding protein AtCBL2 from Arabidopsis thaliana[J]. J Biol Chem, 2003, 278(43):42240-42246.
[50] Gu Z, Ma B, Jiang Y, et al.Expression analysis of the calcineurin B-like gene family in rice(Oryza sativa L.)under environmental stresses[J]. Gene, 2008, 415(1-2):1-12.
[51] Kolukisaoglu U, Weinl S, et al.Calcium sensors and their interacting protein kinases:genomics of the Arabidopsis and rice CBL-CIPK signaling networks[J]. Plant Physiol, 2004, 134(1):43-58.
[52] Hashimoto K, Eckert C, Anschütz U, et al.Phosphorylation of calcineurin B-like(CBL)calcium sensor proteins by their CBL-interacting protein kinases(CIPKs)is required for full activity of CBL-CIPK complexes toward their target proteins[J]. J Biol Chem, 2012, 287(11):7956-7968.
[53] Cuéllar T, Pascaud F, Verdeil J, et al.A grapevine Shaker inward K+ channel activated by the calcineurin B-like calcium sensor 1-protein kinase CIPK23 network is expressed in grape berries under drought stress conditions[J]. Plant J, 2010, 61(1):58-69.
[54] Cuéllar T, Azeem F, et al.Potassium transport in developing fleshy fruits:the grapevine inward K+ channel VvK1. 2 is activated by CIPK-CBL complexes and induced in ripening berry flesh cells[J]. Plant J, 2013, 73(6):1006-1018.
[55] Geiger D, Becker D, Vosloh D, et al.Heteromeric AtKC1·AKT1 channels in Arabidopsis roots facilitate growth under K+-limiting conditions[J]. J Biol Chem, 2009, 284(32):21288-21295.
[56] Ren X, Qi G, Feng H, et al.CalcineurinB-like protein CBL10 directly interacts with AKT1 and modulates K+ homeostasis in Arabidopsis[J]. Plant J, 2013, 74(2):258-266.
[57] Lee SC, Lan WZ, Kim BG, et al.A protein phosphorylation/dephosphorylation network regulates a plant potassium channel[J]. Proc Natl Acad Sci USA, 2007, 104(40):15959-15964.
[58] Lan WZ, Lee SC, Che YF, et al.Mechanistic analysis of AKT1 regulation by the CBL-CIPK-PP2CA interactions[J]. Molecular Plant, 2011, 4(3):527-536.
[59] Salinas M, Duprat F, Heurteaux C, et al.New modulatory α subunits for mammalian shark K+ channels[J]. J Biol Chem, 1997, 272(39):24371-24379.
[60] Jeanguenin L, Alcon C, Duby G, et al.AtKC1 is a general modulator of Arabidopsis inward Shaker channel activity[J]. Plant J, 2011, 67(4):570-582.
[61] Reintanz B, Szyroki A, Ivashikina N, et al.AtKC1, a silent Arabidopsis potassium channel α-subunit modulates root hair K+ influx[J]. Proc Natl Acad Sci USA, 2002, 99(6):4079-4084.
[62] Duby G, Hosy E, Fizames C, et al.AtKC1, a conditionally targeted Shaker-type subunit, regulates the activity of plant K+ channels[J]. Plant J, 2008, 53(1):115-123.
[63] Grefen C, Chen ZH, Honsbein A, et al.A novel motif essential for SNARE interaction with the K+ channel KC1 and channel gating in Arabidopsis[J]. Plant Cell, 2010, 22(9):3076-3092.